Implications of ocean acidification for marine microorganisms from the free-living to the host-associated

Frontiers in Marine Science

Volumn 3, Issue APR, 2016, Pages

  O'Brien, Paul A ^a,b   Morrow, Kathleen M ^b   Willis, Bette L ^a   Bourne, David G ^a,b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Adaptation; Biogeochemical cycle; CO2 Seeps; Coral; Holobiont; Invertebrates; Microorganisms; Ocean acidification

Indexed keywords

EID: 84986584030     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2016.00047     Document Type: Review

References (154)

1. Asplund, M. E., Baden, S. P., Russ, S., Ellis, R. P., Gong, N., and Hernroth, B. E. (2014). Ocean acidification and host-pathogen interactions: blue mussels, Mytilus edulis, encountering Vibrio tubiashii. Environ. Microbiol. 16, 1029-1039. doi: 10.1111/1462-2920.12307
2. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, F. (1983). The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257-263. doi: 10.3354/meps010257
3. Barneah, O., Ben-Dov, E., Kramarsky-Winter, E., and Kushmaro, A. (2007). Characterization of black band disease in Red Sea stony corals. Environ. Microbiol. 9, 1995-2006. doi: 10.1111/j.1462-2920.2007.01315.x
4. Barott, K. L., Rodriguez-Mueller, B., Youle, M., Marhaver, K. L., Vermeij, M. J., Smith, J. E., et al. (2011). Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc. Biol. Sci. 279, 1655-1664. doi: 10.1098/rspb.2011.2155
5. Bayer, T., Arif, C., Ferrier-Pagès, C., Zoccola, D., Aranda, M., and Voolstra, C. R. (2013). Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar. Ecol. Prog. Ser. 479, 75-84. doi: 10.3354/meps10197
6. Beardall, J., and Raven, J. A. (2004). The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologica 43, 26-40. doi: 10.2216/i0031-8884-43-1-26.1
7. Beaufort, L., Probert, I., de Garidel-Thoron, T., Bendif, E. M., Ruiz-Pino, D., Metzl, N., et al. (2011). Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476, 80-83. doi: 10.1038/nature10295
8. Bell, J. J., Davy, S. K., Jones, T., Taylor, M. W., and Webster, N. S. (2013). Could some coral reefs become sponge reefs as our climate changes? Glob. Chang. Biol. 19, 2613-2624. doi: 10.1111/gcb.12212
9. Bengen, D. G., Khoeri, M. M., Marhaeni, B., Radjasa, O. K., Sabdono, A., and Sudoyo, H. (2011). Antifouling activity of bacterial symbionts of seagrasses against marine biofilm-forming bacteria. J. Environ. Protect. 02, 1245-1249. doi: 10.4236/jep.2011.29143
10. Ben-Haim, Y., Thompson, F. L., Thompson, C. C., Cnockaert, M. C., Hoste, B., Swings, J., et al. (2003). Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int. J. Syst. Evol. Microbiol. 53(Pt 1), 309-315. doi: 10.1099/ijs.0.02402-0
11. Bordenstein, S. R., and Theis, K. R. (2015). Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 13:e1002226. doi: 10.1371/journal.pbio.1002226
12. 2 correlates with low concentrations of intracellular dimethylsulfoniopropionate in the sea anemone Anemonia viridis. Ecol. Evol. 4, 441-449. doi: 10.1002/ece3.946
13. Bourne, D., Iida, Y., Uthicke, S., and Smith-Keune, C. (2008). Changes in coral-associated microbial communities during a bleaching event. ISME J. 2, 350-363. doi: 10.1038/ismej.2007.112
14. Bourne, D. G., Muirhead, A., and Sato, Y. (2011). Changes in sulfate-reducing bacterial populations during the onset of black band disease. ISME J. 5, 559-564. doi: 10.1038/ismej.2010.143
15. Bourne, D. G., van der Zee, M. J., Botte, E. S., and Sato, Y. (2013). Sulfur-oxidizing bacterial populations within cyanobacterial dominated coral disease lesions. Environ. Microbiol. Rep. 5, 518-524. doi: 10.1111/1758-2229.12055
16. Bourne, D. G., and Webster, N. S. (2013). "Coral reef bacterial communities," in The Prokaryotes, eds E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (Berlin; Heidelberg: Springer), 163-187
17. Bowen, J. L., Kearns, P. J., Holcomb, M., and Ward, B. B. (2013). Acidification alters the composition of ammonia-oxidizing microbial assemblages in marine mesocosms. Mar. Ecol. Prog. Ser. 492, 1-8. doi: 10.3354/meps10526
18. Boyd, P. W. (2011). Beyond ocean acidification. Nat. Geosci. 4, 273-274. doi: 10.1038/ngeo1150
19. Brading, P., Warner, M. E., Davey, P., Smith, D. J., Achterberg, E. P., and Suggett, D. J. (2011). Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol. Oceanogr. 56, 927-938. doi: 10.4319/lo.2011.56.3.0927
20. Capone, D. G. (2000). "The marine microbial nitrogen cycle," in Microbial Ecology of the Oceans, ed D. L. Kirchman (New York, NY: Wiley-Liss), 455-493
21. Capone, D. G., Burns, J. A., Montoya, J. P., Subramaniam, A., Mahaffey, C., Gunderson, T., et al. (2005). Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Glob. Biogeochem. Cycles 19:GB2024. doi: 10.1029/2004GB002331
22. Capone, D. G., Zehr, L. P., Paerl, H. W., Bergman, B., and Carpenter, E. J. (1997). Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221-1229. doi: 10.1126/science.276.5316.1221
23. Cardini, U., Bednarz, V. N., Foster, R. A., and Wild, C. (2014). Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol. Evol. 4, 1706-1727. doi: 10.1002/ece3.1050
24. Cardini, U., Bednarz, V. N., Naumann, M. S., van Hoytema, N., Rix, L., Foster, R. A., et al. (2015). Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc. Biol. Sci. 282:20152257. doi: 10.1098/rspb.2015.2257
25. Cervino, J. M., Thompson, F. L., Gomez-Gil, B., Lorence, E. A., Goreau, T. J., Hayes, R. L., et al. (2008). The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. J. Appl. Microbiol. 105, 1658-1671. doi: 10.1111/j.1365-2672.2008.03871.x
26. Coelho, F. J., Santos, A. L., Coimbra, J., Almeida, A., Cunha, A., Cleary, D. F., et al. (2013). Interactive effects of global climate change and pollution on marine microbes: the way ahead. Ecol. Evol. 3, 1808-1818. doi: 10.1002/ece3.565
27. Cornwall, C. E., and Hurd, C. L. (2016). Experimental design in ocean acidification research: problems and solutions. ICES J. Mar. Sci. 73, 572-581. doi: 10.1093/icesjms/fsv118
28. Dang, H., and Lovell, C. R. (2016). Microbial surface colonization and biofilm development in marine environments. Microbiol. Mol. Biol. Rev. 80, 91-138. doi: 10.1128/MMBR.00037-15
29. De Beer, D., and Larkum, A. W. D. (2001). Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ. 24, 1209-1217. doi: 10.1046/j.1365-3040.2001.00772.x
30. D'Elia, C. F., and Wiebe, W. J. (1990). "Biogeochemical nutrient cycles in coral-reef ecosystems," in Coral Reefs, ed Z. Dubinsky (Amsterdam: Elsevier), 49-74
31. Denner, E. B., Smith, G. W., Busse, H. J., Schumann, P., Narzt, T., Polson, S. W., et al. (2003). Aurantimonas coralicida gen. nov., sp. nov., the causative agent of white plague type II on Caribbean scleractinian corals. Int. J. Syst. Evol. Microbiol. 53(Pt 4), 1115-1122. doi: 10.1099/ijs.0.02359-0
32. Domingues, A. M., Church, J. A., White, N. J., Gleckler, P. J., Wijffels, S. E., Barker, P. M., et al. (2008). Improved estimates of upper-ocean warming and multidecadal sea level rise. Nature 453, 1090-1094. doi: 10.1038/nature07080
33. Doney, S. C. (2010). The growing human footprint on coastal and open-ocean biogeochemistry. Science 328, 1512-1516. doi: 10.1126/science.1185198
34. 2 problem. Ann. Rev. Mar. Sci. 1, 169-192. doi: 10.1146/annurev.marine.010908.163834
35. Duperron, S., Lorion, J., Samadi, S., Gros, O., and Gaill, F. (2009). Symbioses between deep-sea mussels (Mytilidae: Bathymodiolinae) and chemosynthetic bacteria: diversity, function and evolution. C. R. Biol. 332, 298-310. doi: 10.1016/j.crvi.2008.08.003
36. Ellis, R. P., Widdicombe, S., Parry, H., Hutchinson, T. H., and Spicer, J. I. (2015). Pathogenic challenge reveals immune trade-off in mussels exposed to reduced seawater pH and increased temperature. J. Exp. Mar. Biol. Ecol. 462, 83-89. doi: 10.1016/j.jembe.2014.10.015
37. Erez, J., Reynaud, S., Silverman, J., Schneider, K., and Allemand, D. (2011). "Coral calcification under ocean acidification and global change," in Coral Reefs: An Ecosystem in Transition, eds Z. Dubinsky, and N. Stambler (Springer), 151-176
38. Erwin, P. M., and Thacker, R. W. (2008). Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts. Mol. Ecol. 17, 2937-2947. doi: 10.1111/j.1365-294X.2008.03808.x
39. Fabricius, K. E., De'ath, G., Noonan, S., and Uthicke, S. (2014). Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. Biol. Sci. 281:20132479. doi: 10.1098/rspb.2013.2479
40. Fabricius, K. E., Langdon, C., Uthicke, S., Humphrey, C., Noonan, S., De'ath, G., et al. (2011). Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Chang. 1, 165-169. doi: 10.1038/nclimate1122
41. Fan, L., Liu, M., Simister, R., Webster, N. S., and Thomas, T. (2013). Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J. 7, 991-1002. doi: 10.1038/ismej.2012.165
42. Field, C. B., Behrenfeld, M. J., Randerson, J. T., and Falkowski, P. (1998). Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240. doi: 10.1126/science.281.5374.237
43. Fine, M., and Loya, Y. (2002). Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc. Biol. Sci. 269, 1205-1210. doi: 10.1098/rspb.2002.1983
44. 2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43, 485-496. doi: 10.1111/j.1529-8817.2007.00355.x
45. Gilbert, J. A., Field, D., Swift, P., Newbold, L., Oliver, A., Smyth, T., et al. (2009). The seasonal structure of microbial communities in the Western English Channel. Environ. Microbiol. 11, 3132-3139. doi: 10.1111/j.1462-2920.2009.02017.x
46. Gilbert, J. A., Meyer, F., Jansson, J., Gordon, J., Pace, N., Tiedje, J., et al. (2010). The earth microbiome project: meeting report of the "1st EMP meeting on sample selection and acquisition" at Argonne National Laboratory October 6th 2010. Stand. Genomic Sci. 3, 249-253. doi: 10.4056/aigs.1443528
47. Gilbert, J. A., Steele, J. A., Caporaso, J. G., Steinbruck, L., Reeder, J., Temperton, B., et al. (2012). Defining seasonal marine microbial community dynamics. ISME J. 6, 298-308. doi: 10.1038/ismej.2011.107
48. Giovannoni, S. J., and Stingl, U. (2005). Molecular diversity and ecology of microbial plankton. Nature 437, 343-348. doi: 10.1038/nature04158
49. Godbold, J. A., and Calosi, P. (2013). Ocean acidification and climate change: advances in ecology and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20120448. doi: 10.1098/rstb.2012.0448
50. Goodwin, C., Rodolfo-Metalpa, R., Picton, B., and Hall-Spencer, J. M. (2014). Effects of ocean acidification on sponge communities. Mar. Ecol. 35, 41-49. doi: 10.1111/maec.12093
51. Guinotte, J. M., and Fabry, V. J. (2008). Ocean acidification and its potential effects on marine ecosystems. Ann. N.Y. Acad. Sci. 1134, 320-342. doi: 10.1196/annals.1439.013
52. Hall-Spencer, J. M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S. M., et al. (2008). Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96-99. doi: 10.1038/nature07051
53. 2-rich vent. Environ. Microbiol. Rep. 7, 516-525. doi: 10.1111/1758-2229.12282
54. Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., et al. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742. doi: 10.1126/science.1152509
55. Hutchins, D. A. (2011). Forecasting the rain ratio. Nature 476, 41-42. doi: 10.1038/476041a
56. 2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293-1304. doi: 10.4319/lo.2007.52.4.1293
57. 2 world. Science 320, 336-340. doi: 10.1126/science.1154122
58. Jin, P., Gao, K., and Beardall, J. (2013). Evolutionary responses of a coccolithophorid Gephyrocapsa oceanica to ocean acidification. Evolution 67, 1869-1878. doi: 10.1111/evo.12112
59. Joint, I., Doney, S. C., and Karl, D. M. (2011). Will ocean acidification affect marine microbes? ISME J. 5, 1-7. doi: 10.1038/ismej.2010.79
60. Jones, G. P., McCormick, M. I., Srinivasan, M., and Eagle, J. V. (2004). Coral decline threatens fish biodiversity in marine reserves. Proc. Natl. Acad. Sci. U.S.A. 101, 8251-8253. doi: 10.1073/pnas.0401277101
61. Jones, R. J., Bowyer, J., Hoegh-Guldberg, O., and Blackall, L. L. (2004). Dynamics of a temperature-related coral disease outbreak. Mar. Ecol. Prog. Ser. 281, 63-77. doi: 10.3354/meps281063
62. Karl, D. M., and Church, M. J. (2014). Microbial oceanography and the Hawaii Ocean Time-series programme. Nat. Rev. Microbiol. 12, 699-713. doi: 10.1038/nrmicro3333
63. Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. doi: 10.1007/BF01731581
64. Kline, D. I., Kuntz, N. M., Breitbart, M., Knowlton, N., and Rohwer, F. (2006). Role of elevated organic carbon levels and microbial activity in coral mortality. Mar. Ecol. Prog. Ser. 314, 119-125. doi: 10.3354/meps314119
65. 2 and diurnal changes. Limnol. Oceanogr. 54, 548-559. doi: 10.4319/lo.2009.54.2.0548
66. Krause, E., Wichels, A., Giménez, L., and Gerdts, G. (2013). Marine fungi may benefit from ocean acidification. Aquat. Microbial. Ecol. 69, 59-67. doi: 10.3354/ame01622
67. Krause, E., Wichels, A., Gimenez, L., Lunau, M., Schilhabel, M. B., and Gerdts, G. (2012). Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS ONE 7:e47035. doi: 10.1371/journal.pone.0047035
68. 2, pH and light. Mar. Ecol. Prog. Ser. 117, 159-172. doi: 10.3354/meps117159
69. Kushmaro, A., Banin, E., Loya, Y., Stackebrandt, E., and Rosenberg, E. (2001). Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int. J. Syst. Evol. Microbiol. 51, 1383-1388. doi: 10.1099/00207713-51-4-1383
70. Langer, G., Nehrke, G., Probert, I., Ly, J., and Ziveri, P. (2009). Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosci. Discuss. 6, 4361-4383. doi: 10.5194/bgd-6-4361-2009
71. Larkum, A. W. D., Kennedy, I. R., and Muller, W. J. (1988). Nitrogen fixation on a coral reef. Mar. Biol. 98, 143-155. doi: 10.1007/BF00392669
72. Leblud, J., Moulin, L., Batigny, A., Dubois, P., and Grosjean, P. (2014). Technical note: artificial coral reef mesocosms for ocean acidification investigations. Biogeosci. Discuss. 11, 15463-15505. doi: 10.5194/bgd-11-15463-2014
73. Lee, S. T., Davy, S. K., Tang, S. L., Fan, T. Y., and Kench, P. S. (2015). Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress. FEMS Microbiol. Ecol. 91:fiv142. doi: 10.1093/femsec/fiv142
74. Lema, K. A., Bourne, D. G., and Willis, B. L. (2014b). Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora. Mol. Ecol. 23, 4682-4695. doi: 10.1111/mec.12899
75. Lema, K. A., Willis, B. L., and Bourne, D. G. (2012). Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl. Environ. Microbiol. 78, 3136-3144. doi: 10.1128/AEM.07800-11
76. Lema, K. A., Willis, B. L., and Bourne, D. G. (2014a). Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ. Microbiol. 16, 3345-3359. doi: 10.1111/1462-2920.12366
77. Lesser, M. P., and Blakemore, R. P. (1990). Description of a novel symbiotic bacterium from the brittle star, Amphipholis squamata. Appl. Environ. Microbiol. 56, 2436-2440
78. Lesser, M. P., Mazel, C. H., Gorbunov, M. Y., and Falkowski, P. G. (2004). Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305, 997-1000. doi: 10.1126/science.1099128
79. 2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Chang. Biol. 13, 531-538. doi: 10.1111/j.1365-2486.2006.01314.x
80. Li, J., Chen, Q., Long, L. J., Dong, J., Yang, J., and Zhang, S. (2014). Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci. Rep. 4:7320. doi: 10.1038/srep07320
81. Littman, R. A., Bourne, D. G., and Willis, B. L. (2010). Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol. Ecol. 19, 1978-1990. doi: 10.1111/j.1365-294X.2010.04620.x
82. Liu, J., Weinbauer, M. G., Maier, C., Dai, M., and Gattuso, J. P. (2010). Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat. Microbial. Ecol. 61, 291-305. doi: 10.3354/ame01446
83. Lohbeck, K. T., Riebesell, U., and Reusch, T. B. H. (2012). Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5, 346-351. doi: 10.1038/ngeo1441
84. Luna, G. M., Bongiorni, L., Gili, C., Biavasco, F., and Danovaro, R. (2010). Vibrio harveyi as a causative agent of the White Syndrome in tropical stony corals. Environ. Microbiol. Rep. 2, 120-127. doi: 10.1111/j.1758-2229.2009.00114.x
85. McFall-Ngai, M. J. (1999). Consequences of evolving with bacterial symbionts: insights from the Squid-Vibrio associations. Annu. Rev. Ecol. Syst. 30, 235-256. doi: 10.1146/annurev.ecolsys.30.1.235
86. Meron, D., Atias, E., Iasur Kruh, L., Elifantz, H., Minz, D., Fine, M., et al. (2011). The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5, 51-60. doi: 10.1038/ismej.2010.102
87. Meron, D., Rodolfo-Metalpa, R., Cunning, R., Baker, A. C., Fine, M., and Banin, E. (2012). Changes in coral microbial communities in response to a natural pH gradient. ISME J. 6, 1775-1785. doi: 10.1038/ismej.2012.19
88. Moberg, F., and Folke, C. (1999). Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215-233. doi: 10.1016/S0921-8009(99)00009-9
89. Montoya, J. P., Holl, C. M., Zehr, J. P., Hansen, A., Villareal, T. A., and Capone, D. G. (2004). High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027-1031. doi: 10.1038/nature02824
90. Moran, M. A., González, J. M., and Kiene, R. P. (2003). Linking a bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group. Geomicrobiol. J. 20, 375-388. doi: 10.1080/01490450303901
91. Moran, N. A., and Sloan, D. B. (2015). The hologenome concept: helpful or hollow? PLoS Biol. 13:e1002311. doi: 10.1371/journal.pbio.1002311
92. Morrow, K. M., Bourne, D. G., Humphrey, C., Botte, E. S., Laffy, P., Zaneveld, J., et al. (2014). Natural volcanic CO seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J. 9, 894-908. doi: 10.1038/ismej.2014.188
93. Morrow, K. M., Moss, A. G., Chadwick, N. E., and Liles, M. R. (2012). Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl. Environ. Microbiol. 78, 6438-6449. doi: 10.1128/AEM.01162-12
94. Neave, M. J., Michell, C. T., Apprill, A., and Voolstra, C. R. (2014). Whole-genome sequences of three symbiotic Endozoicomonas strains. Genome Announc. 2, e00802-e00814. doi: 10.1128/genomeA.00802-14
95. Nelson, C. E., Goldberg, S. J., Wegley, L. K., Haas, A. F., Smith, J. E., Rohwer, F., et al. (2013). Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J. 7, 962-979. doi: 10.1038/ismej.2012.161
96. Noonan, S. H., and Fabricius, K. E. (2016). Ocean acidification affects productivity but not the severity of thermal bleaching in some tropical corals. ICES J. Mar. Sci. 73, 715-726. doi: 10.1093/icesjms/fsv127
97. Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., et al. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681-686. doi: 10.1038/nature04095
98. Partensky, F., Blanchot, J., and Vaulot, D. (1999). Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. Bull. Inst. Oceanogr. Monaco 19, 457-476
99. Patterson, K. L., Porter, J. W., Ritchie, K. B., Polson, S. W., Mueller, E., Peters, E. C., et al. (2002). The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl. Acad. Sci. U.S.A. 99, 8725-8730. doi: 10.1073/pnas.092260099
100. Pearson, P. N., and Palmer, M. R. (2000). Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406, 695-699 doi: 10.1038/35021000
101. Pollock, F. J., Lamb, J. B., Field, S. N., Heron, S. F., Schaffelke, B., Shedrawi, G., et al. (2014). Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS ONE 9:e102498. doi: 10.1371/journal.pone.0102498
102. Pomeroy, L. R., Williams, P. J., Azam, F., and Hobbie, J. E. (2007). The microbial loop. Oceanography 20, 28-33. doi: 10.5670/oceanog.2007.45
103. Pommerening-Roser, A., and Koops, H. P. (2005). Environmental pH as an important factor for the distribution of urease positive ammonia-oxidizing bacteria. Microbiol. Res. 160, 27-35. doi: 10.1016/j.micres.2004.09.006
104. Rädecker, N., Meyer, F. W., Bednarz, V. N., Cardini, U., and Wild, C. (2014). Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix. Mar. Ecol. Prog. Ser. 511, 297-302. doi: 10.3354/meps10912
105. Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J., and Wild, C. (2015). Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 23, 490-497. doi: 10.1016/j.tim.2015.03.008
106. Raina, J. B., Dinsdale, E. A., Willis, B. L., and Bourne, D. G. (2010). Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 18, 101-108. doi: 10.1016/j.tim.2009.12.002
107. Raina, J. B., Tapiolas, D. M., Foret, S., Lutz, A., Abrego, D., Ceh, J., et al. (2013). DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502, 677-680. doi: 10.1038/nature12677
108. Raina, J. B., Tapiolas, D., Willis, B. L., and Bourne, D. G. (2009). Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 75, 3492-3501. doi: 10.1128/AEM.02567-08
109. Rasoulouniriana, D., Siboni, N., Ben-Dov, E., Kramarsky-Winter, E., Loya, Y., and Kushmaro, A. (2009). Pseudoscillatoria coralii gen. nov., sp. nov., a cyanobacterium associated with coral black band disease (BBD). Dis. Aquat. Organ 87, 91-96. doi: 10.3354/dao02089
110. Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I., and Rosenberg, E. (2006). The coral probiotic hypothesis. Environ. Microbiol. 8, 2068-2073. doi: 10.1111/j.1462-2920.2006.01148.x
111. Rhein, M., Rintoul, S. R., Aoki, S., Campos, E., Chambers, D., Feely, R. A., et al. (2013). "Observations: ocean," in Climate Change 2013: The Physical Science Basis. Intergovernmental Panel on Climate Change, Working Group I Contribution to the IPCC Fifth Assessment Report (AR5) (New York, NY: Cambridge Univ Press)
112. 2 ocean. Nature 450, 545-548. doi: 10.1038/nature06267
113. 2. Nature 407, 364-367. doi: 10.1038/35030078
114. Ritchie, K. B. (2006). Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322, 1-14. doi: 10.3354/meps322001
115. 2. Science 350, 1533-1537. doi: 10.1126/science.aaa8026
116. Roeselers, G., and Newton, I. L. (2012). On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl. Microbiol. Biotechnol. 94, 1-10. doi: 10.1007/s00253-011-3819-9
117. Rohwer, F., Seguritan, V., Azam, F., and Knowlton, N. (2002). Diverstiy and distribution of coral-associated bacteria Mar. Ecol. Prog. Ser. 243, 1-10. doi: 10.3354/meps243001
118. Rosenberg, E., Koren, O., Reshef, L., Efrony, R., and Zilber-Rosenberg, I. (2007). The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355-362. doi: 10.1038/nrmicro1635
119. Royal Society (2005). Ocean Acidification due to Increasing Atmospheric Carbon Dioxide. Document 12/05, Royal Society (London)
120. Sand-Jensen, K. A. J. (1977). Effect of epiphytes on eelgrass photosynthesis. Aquat. Bot. 3, 55-63. doi: 10.1016/0304-3770(77)90004-3
121. Sato, Y., Bourne, D. G., and Willis, B. L. (2009). Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef, Australia). Proc. Biol. Sci. 276, 2795-2803. doi: 10.1098/rspb.2009.0481
122. Sato, Y., Willis, B. L., and Bourne, D. G. (2010). Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME J. 4, 203-214. doi: 10.1038/ismej.2009.103
123. Schlüter, L., Lohbeck, K. T., Gutowska, M. A., Gröger, J. P., Riebesell, U., and Reusch, T. B. H. (2014). Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat. Clim. Change 4, 1024-1030. doi: 10.1038/nclimate2379
124. Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., et al. (2012). Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564-576. doi: 10.1038/ismej.2011.116
125. Sett, S., Bach, L. T., Schulz, K. G., Koch-Klavsen, S., Lebrato, M., and Riebesell, U. (2014). Temperature modulates coccolithophorid sensitivity of growth, photosynthesis and calcification to increasing seawater pCO(2). PLoS ONE 9:e88308. doi: 10.1371/journal.pone.0088308
126. Shashar, N., Feldstein, T., Cohen, Y., and Loya, Y. (1994). Nitrogen fixation (acetylene reduction) on a coral reef. Coral Reefs 13, 171-174. doi: 10.1007/BF00301195
127. Smith, J. E., Shaw, M., Edwards, R. A., Obura, D., Pantos, O., Sala, E., et al. (2006). Indirect effects of algae on coral: algae mediated, microbe induced coral mortality. Ecol. Lett. 9, 835-845. doi: 10.1111/j.1461-0248.2006.00937.x
128. Steinberg, D. K., Carlson, C. A., Bates, N. R., Johnson, R. J., Michaels, A. F., and Knap, A. H. (2001). Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep Sea Res. II 48, 1405-1447. doi: 10.1016/S0967-0645(00)00148-X
129. Strahl, J., Stolz, I., Uthicke, S., Vogel, N., Noonan, S. H., and Fabricius, K. E. (2015). Physiological and ecological performance differs in four coral taxa at a volcanic carbon dioxide seep. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 184, 179-186. doi: 10.1016/j.cbpa.2015.02.018
130. Sunagawa, S., DeSantis, T. Z., Piceno, Y. M., Brodie, E. L., DeSalvo, M. K., Voolstra, C. R., et al. (2015). Structure and function of the global ocean microbiome. Science 348:1261359. doi: 10.1126/science.1261359
131. Sunagawa, S., DeSantis, T. Z., Piceno, Y. M., Brodie, E. L., DeSalvo, M. K., Voolstra, C. R., et al. (2009). Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512-521. doi: 10.1038/ismej.2008.131
132. Sunagawa, S., Woodley, C. M., and Medina, M. (2010). Threatened corals provide underexplored microbial habitats. PLoS ONE 5:e9554. doi: 10.1371/journal.pone.0009554
133. Sunda, W., Kieber, D. J., Kiene, R. P., and Huntsman, S. (2002). An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317-320. doi: 10.1038/nature00851
134. Sweet, M. J., Bythell, J. C., and Nugues, M. M. (2013). Algae as reservoirs for coral Pathogens. Plos One, 8:e69717. doi: 10.1371/journal.pone.0069717
135. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 doi: 10.1093/molbev/mst197
136. Thompson, F. L., Barash, Y., Sawabe, T., Sharon, G., Swings, J., and Rosenberg, E. (2006). Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef. Int. J. Syst. Evol. Microbiol. 56(Pt 2), 365-368. doi: 10.1099/ijs.0.63800-0
137. Tracy, A., Koren, O., Douglas, N., Weil, E., and Harvell, D. (2015). Persistent shifts in caribbean coral microbiota are linked to the 2010 warm thermal anomaly. Environ. Microbiol. Rep. 7, 471-479. doi: 10.1111/1758-2229.12274
138. Vega Thurber, R., Willner-Hall, D., Rodriguez-Mueller, B., Desnues, C., Edwards, R. A., Angly, F., et al. (2009). Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11, 2148-2163. doi: 10.1111/j.1462-2920.2009.01935.x
139. Venn, A. A., Tambutte, E., Lotto, S., Zoccola, D., Allemand, D., and Tambutte, S. (2009). Imaging intracellular pH in a reef coral and symbiotic anemone. Proc. Natl. Acad. Sci. U.S.A. 106, 16574-16579. doi: 10.1073/pnas.0902894106
140. Ward, B. B. (2000). "Nitrification and the marine nitrogen cycle," in Microbial Ecology of the Ocean, ed D. L. Kirchman (New York, NY: Wiley-Liss), 427-454
141. Webster, N., and Hill, R. (2007). "Chapter 5 Vulnerability of marine microbes on the Great Barrier Reef to climate change," in Climate Change and the Great Barrier Reef: A Vulnerability Assessment, eds J. E. Johnson and P. A. Marshall (Townsville: Great Barrier Reef Marine Park Authority and Australian Greenhouse Office), 97-120
142. Webster, N. S., Cobb, R. E., and Negri, A. P. (2008). Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2, 830-842. doi: 10.1038/ismej.2008.42
143. Webster, N. S., Negri, A. P., Botté, E. S., Laffy, P. W., Flores, F., Noonan, S., et al. (2016). Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6:19324. doi: 10.1038/srep19324
144. Webster, N. S., Negri, A. P., Flores, F., Humphrey, C., Soo, R., Botte, E. S., et al. (2013a). Near-future ocean acidification causes differences in microbial associations within diverse coral reef taxa. Environ. Microbiol. Rep. 5, 243-251. doi: 10.1111/1758-2229.12006
145. Webster, N. S., and Taylor, M. W. (2012). Marine sponges and their microbial symbionts: love and other relationships. Environ. Microbiol. 14, 335-346. doi: 10.1111/j.1462-2920.2011.02460.x
146. Webster, N. S., Uthicke, S., Botté, E. S., Flores, F., and Negri, A. P. (2013b). Ocean acidification reduces induction of coral settlement by crustose coralline algae. Glob. Chang. Biol. 19, 303-315. doi: 10.1111/gcb.12008
147. Webster, N. S., Webb, R. I., Ridd, M. J., Hill, R. T., and Negri, A. P. (2001). The effects of copper on the microbial community of a coral reef sponge. Environ. Microbiol. 3, 19-31. doi: 10.1046/j.1462-2920.2001.00155.x
148. Welsh, E. A., Liberton, M., Stockel, J., Loh, T., Elvitigala, T., Wang, C., et al. (2008). The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle. Proc. Natl. Acad. Sci. U.S.A. 105, 15094-15099. doi: 10.1073/pnas.0805418105
149. White, A. T., Vogt, H. P., and Arin, T. (2000). Philippine coral reefs under threat: the economic losses caused by reef destruction. Mar. Pollut. Bull. 40, 598-605. doi: 10.1016/S0025-326X(00)00022-9
150. Williams, G. J., Price, N. N., Ushijima, B., Aeby, G. S., Callahan, S., Davy, S. K., et al. (2014). Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease. Proc. Biol. Sci. 281:20133069. doi: 10.1098/rspb.2013.3069
151. Yang, C. S., Chen, M. H., Arun, A. B., Chen, C. A., Wang, J. T., and Chen, W. M. (2010). Endozoicomonas montiporae sp. nov., isolated from the encrusting pore coral Montipora aequituberculata. Int. J. Syst. Evol. Microbiol. 60(Pt 5), 1158-1162. doi: 10.1099/ijs.0.014357-0
152. Yost, D. M., Jones, R. J., and Mitchelmore, C. L. (2010). Alterations in dimethylsulfoniopropionate (DMSP) levels in the coral Montastraea franksi in response to copper exposure. Aquat. Toxicol. 98, 367-373. doi: 10.1016/j.aquatox.2010.03.005
153. Zilber-Rosenberg, I., and Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723-735. doi: 10.1111/j.1574-6976.2008.00123.x
154. 2. Glob. Biogeochem. Cycles 15, 507-516. doi: 10.1029/2000GB001321